Spanish Journal of Agricultural Research 17 (4), e10R01, 13 pages (2019) eISSN: 2171-9292 https://doi.org/10.5424/sjar/2019174-15073 Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)

REVIEW ARTICLE OPEN ACCESS

The microbiome and biological control of weeds: A review Anupma Dahiya (Dahiya, A), Kavita Chahar (Chahar, K) and Satyavir S. Sindhu (Sindhu, SS) CCS Haryana Agricultural University, Hisar, 125 004, India.

Abstract The productivity of important grain crops wheat, rice and maize is adversely affected by various biotic and abiotic stresses. Weeds and phytopathogens are the major biotic stresses involved in biomass reduction and yield losses of these cereal crops. Various weeds compete with crop plants for natural resources viz. light, moisture, nutrients and space, and cause yield losses to agricultural produce. Weeds also increase harvesting costs and reduce quality of the farm produce. Weed management strategies include crop rotation, mechanical weeding or treatment with different herbicides. Although, sprays of different herbicides control various destructive weeds but their excessive use is environmentally unsafe and uneconomic. Indiscriminate use of these agrochemicals for weed control has resulted into considerable pollution of , groundwater and atmosphere. Therefore, effective biological weed management is an attractive approach for achieving the increased crop production to meet the food demands of the escalating global population. Many and fungi have been identified from the plant , which suppress the growth of weeds. The production of indole acetic acid, aminolevulinic acid, toxins and hydrogen cyanide has been correlated with the growth suppression of various weeds. Interestingly, inoculation with bioherbicides results in creation of biased rhizosphere leading to resource partitioning of nutrients towards growth stimulation of crop plants. Thus, inoculation of plants with bioherbicides has been found to increase germination percentage, seedling vigor, root and shoot growth, seed weight and increased grain, fodder and fruit yields. These environment-friendly biocontrol strategies for management of weeds are highly compatible with the sustainable agriculture. Additional keywords: rhizosphere bacteria; natural resources; biotic stresses; resource partitioning; growth promotion; bioherbicides; sustainable agriculture. Abbreviations used: 2,4-D (2,-4-dichlorophenoxyacetic acid); 2,4,5-T (2,-4,-5-trichlorophenoxyacetic acid); AAL (Alternaria alternata f. sp. lycopersici toxin); ALA (δ-aminolevulinic acid); DRB (deleterious rhizosphere bacteria); HCN (hydrogen cyanide); IAA (indole acetic acid); ISR (induced systemic resistance); PGPR (plant growth promoting rhizosphere bacteria); RDW (root dry weight); SDW (shoot dry weight); VOC (volatile organic compounds). Authors’ contributions: Concept and design: SSS. Compiled the information: AD and KC. All authors analyzed the data, wrote the paper and approved the final manuscript. Citation: Dahiya, A; Chahar, K; Sindhu, SS (2019). The rhizosphere microbiome and biological control of weeds: A review. Spanish Journal of Agricultural Research, Volume 17, Issue 4, e10R01. https://doi.org/10.5424/sjar/2019174-15073 Received: 26 Apr 2019. Accepted: 23 Dec 2019. Copyright © 2019 INIA. This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC-by 4.0) License.

Funding agencies/Institutions Project / Grant University Grant Commission, New Delhi (Rajiv Gandhi National Fellowship for RGNF-2015-17-SC-HAR-5228 SC candidate to Anupama Dahiya as Junior Research Fellow)

Competing interests: The authors have declared that no competing interests exist. Correspondence should be addressed to Satyavir S. Sindhu: [email protected]; [email protected]

Introduction variability in yield losses among the different locations (states) in case of direct-seeded rice (15-66%) and ma­ Weeds adversely affect the production of the world's ize (18-65%). Soltani et al. (2016) estimated average most important food and cash crops. Assessment of yield loss in corn as 50%, i.e., 148 million tonnes of corn yield losses due to weeds were estimated at 26-29% for valued at over USD 26.7 billion annually in the United soybean, wheat and cotton, and 31, 37 and 40% for maize, States and Canada. rice and potatoes, respectively (Oerke, 2006). Significant Weeds are the silent robbers of plant nutrients, differences in yield losses were observed between di­ soil moisture, solar energy and also occupy the space fferent locations, crops and soil types. For example, Bhan which would otherwise be available to the main crop. et al. (1999) estimated a 31.5% of reduction in yield by Moreover, weeds harbour insect-pests and disease- weeds, whereas Gharde et al. (2018) reported greater causing or­ganisms, exert adverse allelopathic effects, 2 Anupma Dahiya, Kavita Chahar and Satyavir S. Sindhu

reduce quality of farm produce and increase the cost toxin produced by the pathogen Alternaria alternata of production. Seeds of weeds can stay in the soil for f. sp. lycopersici has been found to inhibit a range of several years until conditions are favorable for their weed species and has been patented as an herbicide germination. After germination, weed plants grow fast, (Abbas et al., 1995). Other allelochemicals produced rapidly establish weed populations and soon reach the by microorganisms such as indole acetic acid (IAA), δ- flowering phase. They again produce numerous seeds, aminolevulinic acid (ALA), glycoproteins and mellein which are easily dispersed over long distances. Some have also been reported to reduce the germination and weeds produce vegetative reproduction organs that help development of weeds (Mejri et al., 2010; Adetunji et them to survive in . al., 2018; Radhakrishnan et al., 2018). Moreover, ino­ The major prevalent dicot weeds include bathua culation of soil with deleterious microorganisms (Chenopodium album), gazari (Fumaria parviflora), (bio­control agents) may suppress weed growth by krishnneel (Anagallis arvensis), chetri (Vicia sativa), production of hydrogen cyanide (Zeller et al., 2007). senji (Melilotus indicus), matari (Lathyrus aphaca) and These rhizosphere microorganisms could be exploited satyanashi (Argemone mexicana). Likewise, monocot for development of bioherbicides as ecofriendly weeds viz. kanki/gullidanda/ mandusi (Phalaris minor), technology for management of weeds in sustainable­ wild oats (Avena ludoviciana, Avena fatua), piazi agriculture. In addition, in-depth understanding of me­ (Asphodelus tenuifolius) etc., impose serious problems chanisms and factors involved in crop-weed competitive in wheat fields. Avena fatua is one of the most eco­ interactions is required to develop cost-effective and nomically harmful annual grass weed in North America, sustainable weed management strategies (Swanton et Europe and Australia especially in grain crops such as al., 2015; Adetunji et al., 2019). barley, oat and wheat. Similarly, P. minor is another troublesome weed of wheat in India, Pakistan, USA, Canada, Africa, Australia, France, Iran and Mexico. It Rhizosphere and plant microbiome may cause 25-80% reduction in wheat yield (Chhokar et al., 2009). Herbicides such as isoproturon, clodinafop- The rhizosphere is a region of rich microbial di­ propargyl, fenoxaprop, pinoxaden, Accord plus (feno­ versity, which is influenced by plant roots through xaprop + metribuzin), sulfosulfuron and Atlantis (meso + rhizodeposition of root exudates, plant mucilage and iodosulfuron) are applied for control of common weeds. sloughed cells (Mohanram & Kumar, 2019). Root exu­ Nevertheless, the application of chemical herbicides dates are the key determinants of rhizosphere microbiome leaves residues that contaminate water, soils and food structure. These root exudates contain a variety of com­ crops, and in some cases results in the development of pounds, predominately organic acids and sugars, but herbicide resistance in many weed biotypes. Therefore, also contain amino acids, fatty acids, vitamins, growth it is imperative to explore various biocontrol appro­ factors, hormones and antimicrobial compounds (Sindhu aches that are ecofriendly for the control of weeds. et al., 2017). The composition of root exudates varies Naturally-occurring rhizosphere microorganisms have between plant species and cultivars, plant age and the the potential to suppress the weed growth through al­ developmental stage. The physico-chemical properties teration of the rhizosphere ecosystem (Charudattan of soils may also directly affect the growth of specific & Dinoor, 2000; Mohan Babu et al., 2003; Adetunji et microbes by creating niche environments that benefit al., 2019). These rhizosphere bacteria colonize the certain types of microbes and influence the availability root surface of weed seedlings and suppress the growth of plant root exudates. For instance, soil pH and nutrient­ of weed plants by reducing weed density, biomass availability (e.g. carbon, nitrogen, phosphate) have been and its seed production (Kremer & Kennedy, 1996). found to affect the abundance of crop pathogenic bact­ Many rhizobacterial strains including eria, fungi and nematodes as well as beneficial microbes aeruginosa, Flavobacterium spp., Erwinia herbicola, (Lareen et al., 2016). Recent advances in plant-microbe Alcaligenes spp., Xanthomonas campestris pv. poannua, interactions revealed that plants are able to mani­ Pseudomonas syringae pv. tagetis and P. syringae pv. pulate their rhizosphere microbiome, when different phaseolicola have been exploited as foliar bioherbicides, plant species are grown on the same soil (Berendsen whereas P. fluorescens, Xanthomonas spp., Enterobacter et al., 2012; Chaparro et al., 2012; Turner et al., 2013). sp and Erwinia herbicola have been developed as Rhizosphere engineering reduce the incidence of plant soil application bioherbicides (Kremer, 2000; Sindhu diseases and invasion of pathogens, the use of chemical et al., 2018; Adetunji et al., 2019). Some deleterious inputs and emissions of greenhouse gases resulting in rhizobacteria (DRB) and fungi cause damage to the more sustainable agricultural practices for the benefit of weed plants through the production of phytotoxins that the whole ecosystem (Zorner et al., 2018). The effect are absorbed by the plant roots. For example, the AAL of soil and plants on the composition of rhizosphere

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communities has been reviewed recently and the 8% isolates only) were found to inhibit root growth of presence or loss of specific microbial hubs under certain downy brome on agar, but did not affect root growth of environmental distractions could be critical for soil winter wheat. Under nonsterile soil conditions, only six fertility and plant health (Hunter, 2016; Igiehon & isolates inhibited the growth of downy brome. Growth Babalola, 2018). Certain microbial hubs in the plant of downy brome weed in the field was suppressed by rhizosphere contribute towards improving nutrient up­ 31 to 53% by spraying (at a population density of 108 take or effectiveness of biocontrol agents and mediating colony forming units m-2) of only two isolates. Whereas, defense signals among plants (van der Heijden & the spraying of these isolates increased the yield of Hartmann, 2016) (Fig. 1). winter wheat by 18-35%, under field conditions. Boyetchko (1997) evaluated the efficacy of DRB for biological control of downy brome (Bromus tectorum), Microorganisms involved in biocontrol green foxtail (Setaria viridis) and wild oats (Avena of weeds fatua). Over 100 isolates with 280% suppression to root growth of these weeds in laboratory bioassays were Various soil microorganisms have been characteri­ ­zed, selected as potential biological control agents. Kennedy which increase the nutrient uptake capacity and water use et al. (2001) isolated Pseudomonas fluorescens strain efficiency of crop plants for enhancing foodtion produc­ D7 (P. f. D7; NRRL B-18293) that inhibited growth of (Armada et al., 2014; Pii et al., 2015; Sindhu et al., 2019). downy brome (Bromus tectorum L. Brote). In the agar These microorganisms may be used to enhance soil fertility plate bioassay, all accessions of downy brome were and plant health without environmental contamination inhibited by P. fluorescens strain D7. Root growth of (Sharma & Sindhu, 2019) and are termed as plant growth seven Bromus spp. was inhibited on an average of 87% promoting rhizobacteria (PGPR). These PGPR include compared with that of controls in the agar plate bioassay. bacterial genera such as Agro­bacterium, Allo­rhizobium, Inhibition in plant–soil bioassays was limited to downy Art­hrobacter, Azospirillum, Azotobacter, Bacillus, Brad­ brome, indicating the application of P. fluorescens D7 as yrhizobium, Burkholderia, Chromobacterium, Erwi­nia, a biocontrol agent that will not harm nontarget species. Mesorhizobium, Micrococcus, Pseudomonas, Rhi­zobium Flores-Vargas & O’Hara (2006) isolated bacteria from and Serratia, which either exist in the rhizosphere, on the the rhizosphere, rhizoplane and endorhizosphere of rhizoplane or in the spaces between the cells of root cor­ seedlings and mature plants of wild radish (Raphanus tex (Viveros et al., 2010; Ahemad & Kibret, 2014). These raphanistrum), annual ryegrass (Lolium rigidum) microbes provide fixed nitrogen,­ solubilized phosphorus and capeweed (Arctotheca calendula) growing in vi­ and other nutrients to the plants (Bhattacharyya & Jha, neyards in the Swan Valley, Western Australia. A total 2012). of 442 strains were screened in the glasshouse for de­ Fluorescent and nonfluorescent pseudomonads, leterious effects on annual ryegrass, wild radish, gra­ Erwinia herbicola, Alcaligenes spp. and Flavobac­ terium spp., were isolated from seedlings of seven economically important weeds (Kremer et al., 1990). Using an Escherichia coli indicator bioassay, only 18% of all isolates were found potentially phytopathogenic and 35-65% of the isolates inhibited growth in seedling assays, depending on the weed host. Antibiosis was found most prevalent among isolates of fluorescent Pseudomonas spp., the activity of which was due to siderophore production­ in over 75% of these isolates. Competitive root colonization was reported as ano­ ther important criterion for development of effective weed biocontrol agents (Kremer et al., 1990). In Improved plant growth addition, differential colonization of roots may result in selectivity of these allelopathic bacteria in terms of their promotion or growth retardation effects, thereby enabling more targeted control of weeds (Kennedy et al., 2001). Differential inhibition of downy brome (Bromus tectorum) and winter wheat was reported by screening of 1000 pseudomonad isolates (Kennedy Figure 1. Rhizosphere microorganisms having bioherbi­ ­ et al., 1991). The filtrates of bacteria-free culture (of cidal activity and plant growth promotion ability.

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pevine rootlings (Vitis vinifera) and the cover crop decrease in root dry weight (RDW) and 31-47% decrease subterranean clover (Trifolium subterraneum). Three in shoot dry weight (SDW) of Chenopodium album at 60 strains specifically inhibited growth of wild radish, and 90 days of plant growth, whereas its inoculation but showed no significant deleterious effects on either showed 122-144% increase in RDW and 124-205% grapevine rootlings or subterranean clover. increase in SDW of wheat under pot house conditions. De Luna et al. (2011) isolated mycobiota associated Inoculation with bacterial isolates­ WHA82 and WHA100 with dormant wild oat (Avena fatua L.) seeds buried for also decreased root and SDW of C. album at both stages six months in a no-till wheat field and evaluated their of observations. caryopsis decay potential. Of the 118 representative Recently, inoculation of phytopathogenic strain La­ isolates tested, only 15% isolates showed caryopsis decay siodiplodia pseudotheobromae showed 56–66% se­ potential. One isolate of Fusarium avenaceum and three lective inhibition against the and Valerianaceae isolates of Fusarium culmorum completely decayed families (Adetunji et al., 2018), whereas Pseudomonas wild oat caryopses within two weeks. Chen et al. (2016) aeruginosa strain C1501 showed significant decrease found that culture filtrate of Streptomyces enissocaesilis in the dry weight of Amaranthus hybridus (pig weed) significantly reduced the germination rate of root pa­ seedlings (Adetunji et al., 2019). ALA-producing Bacillus rasitic weed Orobanche cumana (sunflower broomrape) flexus strain JIM24 was reported to cause 92% reduction both in the seed germination experiment and the co- in root and SDW of Lathyrus aphaca weed under pot culture experiment, with more than 50 and 40% (after house conditions (Phour & Sindhu, 2019). Similarly, cultivation for eight days) growth retardation effect, Lawrancea et al. (2019) isolated a rhizospheric bacterium respectively over the control. In the pot experiment, Pseudomonas aeruginosa strain H6 from the rhizosp­ application of Streptomyces enissocaesilis reduced the here of Momordica charantia. Both, supernatant culture epigaeous number of O. cumana tubercles by 47.5% and crude extract of strain H6 showed high inhibition after 130 days. Abbas et al. (2017) recorded the max­ activity in Pennisetum purpureum, Oryza sativa, Pi­ imum suppression of wild oat due to inoculation with sum sativa and Amaranthus spinosum. strains L9 and T42 followed by strains O010, W9, 7O0 and others. Inoculation with strains O010 and 7O0 caused maximum inhibition of little seed canary Mechanisms involved in bioherbicidal grass, followed by strains L9 and T42. Broad leaved activity dock was maximally­ inhibited by strains W9, T42 and

L9, followed by strains 7O0, O010, T38 and others. Bioherbicides are natural products derived from either Reduction in germination and growth of the weeds living organisms or their natural metabolites, which by allelopathic­ bacteria was attributed to their ability are used to control destructive weed species without for competitive root colonization and production of degrading the environment (Bailey, 2014). Some of phytotoxic metabolites. the rhizospheric bacteria secrete various plant growth Similarly, rhizosphere bacteria obtained from different promoting compounds or toxins, which may inhibit seed crops were screened for antagonism against Amaranthus germination and growth of weed plants (Sindhu et al., hybridus L. (pig weed) and Echinochloa crus-galli (L.) 2018; Adetunji et al., 2019). Various metabolites such as Beauv. (barnyard grass) using the necrosis assay technique­ phytotoxins, , IAA, ALA and HCN produced (Adetunji et al., 2017). Eight rhizosphere bacterial isola­ by bacterial or fungal cells have been found to retard tes (B1–B8) produced different degrees of leaf necrosis growth of weeds (Kim & Rhee, 2012; Park et al., 2015; on target weeds. Isolate B2 showed the highest necrotic Phour et al., 2018; Adetunji et al., 2018; Radhakrishnan activity and was identified as Pseudomonas aeruginosa et al., 2018; Dahiya et al., 2019). using 16S rRNA sequencing technique. Kennedy (2017) found weed-suppressive Pseudomonas fluorescens strains Production of indole acetic acid effective for controlling one or more invasive grass weeds consisting of downy brome (Bro­mus tectorum L.), me­ Phytohormones are the chemical messengers produced dusa head (Taeniatherum caput medusae (L.) Nevski) and by certain plant-associated bacteria that play crucial role jointed goatgrass (Aegilops cylindrica L.). Khandelwal et in different plant-microbe interactions (Costacurta & al. (2018) reported that four rhizobacterial isolates obtai­ Vanderleyden, 1995; Sindhu et al., 2017). Production ned from the rhizosphere of wheat and mustard showed of different phytohormones like IAA, gibberellic acid root growth inhibition of Chenopodium album weed and and cytokinins by the PGPR strains have been reported three bacterial isolates caused shoot growth inhibition to alter root architecture, leading to more adsorption at both 5th and 10th days of seed germination. Inocu­ of nutrients and promotion of plant growth (Malik lation of bacterial isolate MSA39 resulted in 43-53% & Sin­dhu, 2011; Park et al., 2015; Sindhu et al.,

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2017). These phytohormones affect seed growth, time HP72 contribute towards the development of short of flowering, senescence of leaves and fruits, gene root systems and take advantage of root colonization. expression, cellular division and growth. In targeted High amount of IAA production by deleterious cells, phytohormones also regulate cellular processes, rhizobacteria Bradyrhizobium japonicum GD3, isolated pattern formation, vegetative­ and reproductive de­ from soybean rhizosphere, was found to give suppressive velopment and stress responses. effect on growth of morning glory Ipomoea( spp.) weed Indole-3-acetic acid is one of the most common and (Kim & Kremer, 2005). Similarly, growth suppressive most studied auxins (Spaepen et al., 2007). Plant res­ effect on weed great brome Bromus( diandrus Roth.) was ponses to IAA vary from plant to plant in terms of observed by inoculation of Pseudomonas trivialis strain sensitivity. The capacity to produce IAA is wide spread X33d in a mixture of soil/sand/peat (Mejri et al., 2010). among plant associated bacteria (Patten & Glick, 1996; Bromus diandrus plants inoculated with rhizobacterial Kloepper et al., 2007; Mishra et al., 2010; Malik & strain X33d showed low root biomass, short root Sindhu, 2011) and the numbers of IAA-producing systems and low surface area, volume and number of organisms range as high as 80% of total soil bacteria. tips. On the other hand, growth promoting effect was IAA is also involved in regulating the expression of observed on most of the crops, especially durum wheat important compounds in bacteria such as cAMP and (Triticum durum Desf.) by inoculation of Pseudomonas amino acids (Katsy, 1997). IAA production may trivialis strain X33d strain. This growth suppression e­nhance plant growth by enhancing root surface area effect on great brome weed and growth promotion effect through which more of the metabolites can be exuded on durum wheat was attributed to production of IAA by or absorbed as nutrients (Gaudin et al., 1994). P. trivialis strain X33d. Meliani et al. (2017) reported Indole-3-acetic acid has been reported to stimulate that Pseudomonas fluorescens and Pseudomonas plant growth in lower concentrations and in contrast, pu­tida produced IAA in vitro, at concentrations of if the concentration becomes higher, the effect is re­ 89 µg mL-1 and 116 µg mL-1, respectively. High versed and elongation of root and shoot is inhibited. levels of IAA excretion by P. putida gave consistent Natural auxins have modes of action similar to many effects in enhancing the plant growth and vigor index. herbicides that interfere with plant growth such Recently, bacterial isolates BWA18 and RWA52 with as 2, -4 -dich­lo­rophenoxyacetic acid (2, -4 -D) and high IAA production ability (53.80 and 19.18 µg mL-1, 2, -4, -5 -trichlorophenoxyacetic acid (2, -4, -5 -T) (Patten respectively), were found to cause growth inhibition of & Glick, 1996). Nine strains of Klebsiella pneumoniae Avena fatua weed and stimulated the growth of wheat were isolated from rhizosphere of wheat var. Lokwan at 25, 50 and 75 days of observations under pot house (Sachdev et al., 2009) and only six K. pneumoniae strains conditions (Dahiya et al., 2019). showed in vitro IAA production. Inoculation of strains K11 and K42 caused significant gain in root length of Aminolevulinic acid production inoculated moth beans (~ 92.71%) over the control. Pot experiment results indicated that all the six IAA- ALA is a key intermediate in the biosynthesis of producing Klebsiella strains significantly increased tetrapyrroles, such as porphyrins, vitamin B12, chlo­ the root length and shoot height of inoculated wheat rophyll (bacteriochlorophyll) and heme. ALA is a seedlings over the control. Serwar & Kremer (1995) natural photodynamic compound, which is effective as reported that auxins produced in high concentrations a biodegradable herbicide (Sasikala et al., 1994; Phour in the rhizosphere by deleterious rhizobacteria may & Sindhu, 2019) and it has been reported to cause a con­tribute towards reduced root growth of weeds. For stimulating effect on the growth and photosynthesis of example, an Enterobacter taylorae isolate with high crops and vegetables (Sasaki et al., 1993). In plants, auxin-producing potential (72 mg L-1 IAA-equivalents) the ALA concentration is strictly controlled at less than was found to inhibit root growth of field bindweed 50 nmol g-1 fresh weight (Stobart & Ameen-Bukhari, (Convolvulus arvensis L.) by 90.5% when combined 1984). Herbicidal activity has been reported to increase with 1·10-5 M L-tryptophan in comparison with non- accumulation of several chlorophyll intermediates, treated control. Suzuki et al. (2003) isolated an IAA such as protochlorophyllide, protoporphyrin IX and low-producing spontaneous mutant of P. fluorescens Mg-protoporphyrin IX, when plants are treated with HP72LI and the colonization ability of strain HP72 exogenous ALA at relatively high concentrations on the bentgrass root was found higher than that of (5-40 mM). ALA has been applied as a favorable mutant HP72LI. Colonization of strain HP72 on the biodegradable herbicide and insecticide, which is bentgrass root caused root growth reduction, whereas harmless to crops, humans and animals (Beck et al., strain HP72LI did not show such growth reduction. 2007; Bhowmick & Girotti, 2010; Johansson et al., The results suggested that IAA production by strain 2010; Kang et al., 2012).

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Liu et al. (2005) selected, from 36 photosynthetic increased the percentage and rate of germination, bacterial strains, seven strains belonging to Rhodopseu­ plant biomass and nutrient uptake of wheat seedlings domonas sp.; among them, ˈ99-28ˈ showed the highest (Selvakumar et al., 2009). ALA production ability. However, herbicidal activity of Agbodjato et al. (2015) identified five rhizobacterial ALA on several plants has been reported to differ by the species of Bacillus (B. polymyxa, B. pantothenticus, application methods. At low concentrations (0.01-10 mg B. anthracis, B. thuringiensis and B. circulans), three L-1), ALA showed growth-promoting effects on yield of Pseudomonas species (P. cichorii, P. putida and P. several crops (Hotta et al., 1997), whereas it suppressed syringae) and Serratia marcescens. Inoculation of plant growth at higher concentrations (> 2 mM). Zhang these rhizobacteria as biological fertilizers resulted et al. (2006) reported that ALA at low concentrations of into increased maize production. Nandi et al. (2017) 0.3-3 mg L-1 promoted development and growth of found that strain PA23 microtubers in vitro, and enhanced protective functions produced HCN and secreted the antibiotics pyrrolnitrin against oxidative stresses, but application of ALA at and phenazine, together with degradative enzymes and 30 mg L-1 and higher concentrations may induce oxidative siderophores. This strain acted as a biocontrol agent. damage. Hyun & Song (2007) reported production of Similarly, Pseudomonas aeruginosa (HM195190) IAA and ALA by Rhodopseudomonas strains, which strain KC1 isolated from the rhizosphere of castor plants promoted the seed germination and growth of tomato (Ricinus communis) (Lakshmi et al., 2015) was found to plants under axenic conditions. Chaudhary & Sindhu produce cyanide (4.78 nmol L−1) and seed bacterization (2016) found that out of 55 rhizobacterial isolates, only with strain KC1 exhibited significant reduction in root six isolates (HCS7, HCS19, HFS7, HFS9, HFS10 and length and shoot length of weed seedlings (Amaranthus HFS12) showed ALA production varying from 1.3 to spinosus and Portulaca oleracea) in both laboratory 7.0 µg mL-1. Khandelwal et al. (2018) reported that 80% of and glasshouse experiments. However, inoculation of the rhizobacterial isolates from the rhizosphere of wheat strain KC1 was found less inhibitory to the seedlings and mustard produced ALA. More ALA production of Triticum aestivum as compared to weed seedlings. (> 11 µg mL-1) was ob­served in eight bacterial isolates. Other 54 isolates produced ALA ranging from 5 to Phytotoxin production 11 µg mL-1 and nineteen isolates lacked ALA production ability. Phour & Sindhu (2019) reported significant Plant pathogens produce a variety of phytotoxins that reduction (92%) in RDW and SDW of Lathyrus aphaca interfere with plant metabolism, ranging from subtle weed by inoculation of ALA-producing Bacillus flexus effects on gene expression to plant mortality (Walton, strain JIM24 under pot house conditions. 1996). Several bacterial and fungal microorganisms were also found to produce a wide array of phytotoxins Hydrogen cyanide production with the potential to be used as herbicides (Duke et al., 1991). Two phytotoxic metabolites (prehelminthosporal Cyanide production is considered as a major trait of and dihydropore), were isolated from the cultural filtrates rhizobacteria for biological control of weeds (Kremer & of the fungus Bipolaris sp. which showed herbicidal Souissi, 2001), because of its ability to inhibit root cell activity against Sorghum halepense (L.) Pers. (Parmar & metabolism and effective inhibition of the cytochrome Devkumar, 1993). The AAL-toxin (hydroxylated long- oxidase pathway. The HCN production has been found chain alkylamine containing a tricarboxylic acid moiety) to be a common trait of Pseudomonas (88.89%) and produced by Alternaria alternata f. sp. lycopersici has Bacillus (50%) in the rhizospheric soil and plant root been found to act as an effective herbicide on a range nodules (Ahemad & Khan, 2009). Owen & Zdor (2001) of crop and weed species. In susceptible varieties of reported that two strains of cyanogenic rhizobacteria tomatoes, it caused rapid wilting and necrosis (Abbas (Pseudomonas putida and Acidovorax delafieldii), et al., 1995). Similarly, a phytotoxic metabolite trans-4- though significantly inhibited the growth of velvetleaf aminoproline isolated from culture filtrates of Ascochyta (Abutilon theophrasti), did not reduce corn growth caulina was found highly effective in controlling even in the presence of supplemental glycine. Wani Chenopodium album (L.) weed (Evidente et al., 2000). et al. (2007) found that most of the rhizosphere isolates Evidente et al. (2005) isolated a new phytotoxic produced HCN in vitro and stimulated the plant growth. trisubstituted naphthofuroazepinone from the culture On the other hand, Pseudomonas entomophila showed filtrates of Drechslera siccans, named drazepinone biocontrol properties and pathogenicity due to pro­ and characterized as a 3,5,12 a trimethyl- 2,5,5a,12a- duction of HCN (Ryall et al., 2009). The Pseudomonas tetrahydro-1H naphtha [2′,3′:4,5] furo [2,3-b] azepin- fragi strain CS11RH1 (MTCC 8984), produced HCN 2-one. The novel metabolite showed broad-spectrum and the seed bacterization with this strain significantly herbicidal properties at 2 μg μL-1 solution. Another

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mobile phytotoxin mevalocidin, produced by Fusarium & Torgashova (1976) reported that the 2,4- DA056446 and Roselliana DA092917 was reported DAPG showed phytotoxic activity resembling to the to act as a broad spectrum post-emergence herbicide 2,4-D herbicide. Geldanamycin and nigericin, two against grasses and broad-leaved plants (Gerwik et phytotoxic metabolites, were obtained from a strain al., 2013). The cyclic tetrapeptide phytotoxin tentoxin of Streptomyces hygroscopicus and showed significant produced by Alternaria alternata caused phytotoxic pre-emergence activity on proso millet, barnyard grass, damage to both monocot and dicot weeds species and garden cress and giant foxtail. A polyketide secondary therefore showed the potential to be used as bioherbicide metabolite, herboxidiene, produced by Streptomyces (Saxena, 2014). Rath et al. (2018) investigated the role of chromofuscus, showed potent and selective herbicidal volatile organic compounds (VOCs) produced by PGPR activity against weeds but not against wheat (Miller- strains in plant growth promotion. Bacillus subtilis and Wideman et al., 1992). Secondary metabolites iso­ Bacillus amyloliquefaciens strains produced VOCs like lated from Pseudomonas syringae strain 3366 were 3-hydroxy-2-butanone (acetoin) and 2,3-butanediol, found inhibitory to downy brome and these me­ which promoted plant growth, whereas other volatiles tabolites consisted of phenazine-1-carboxylic acid, such as HCN and 3-phenylpropionic acid were found 2-aminophenoxazone and 2-aminophenol (Gealy et al., phytotoxic and inhibited the plant growth. 1996). Similarly, phenazine-type antibiotics produced Adetunji et al. (2018) isolated an active me­ by Pseudomonas fluorescens were also reported to tabolite mellein (a dihydroisocoumarin) from the broth inhibit the root growth of downy brome weed (Gealy of phytopathogenic strain Lasiodiplodia pseudothe­ et al., 1996). obromae and its structural characterization revealed the compound as (R)-8-hydroxy-3-methylisochroman-­ Effect of rhizobacterial inoculation on weed and 1-one. The isolated phytotoxic metabolite from Lasio­ crop plants diplodia pseudotheobromae (at 10 μg μL-1 conc.) showed selective inhibition at 56–66% against the Poaceae and Bacterial species inhabiting the crop rhizosphere have Valerianaceae families. Another bioactive phytotoxin been reported to affect plant growth in either a positive with good herbicidal activity was extracted from Pseu­ or in a negative way. Beneficial effects of rhizosphere domonas aeruginosa strain C1501 and the active bacteria have most often been based on suppression of compound was identified as a 2-(hydroxymethyl) phenol diseases, increased seedling emergence and stimulation (Adetunji et al., 2019). The C1501 strain showed of plant growth along with inhibition of weeds growth significant decrease in the dry weight of Amaranthus (Fig. 2) (Sindhu et al., 2014, 2016; Phour & Sindhu, hybridus (pig weed) seedlings. Lawrancea et al. (2019) 2019). A large array of bacteria, including species of isolated a Pseudomonas aeruginosa strain H6 with Azospirillum, Azotobacter, Art­hrobacter, Bacillus, weedicide efficacy from the rhizosphere of Momordica Enterobacter, Burkholderia, Pa­enibacillus, Pseudo­ charantia. Metabolite identified from strain H6 showed monas and Rhizobium, have been reported to enhance the presence of antifungal and herbicidal compounds. plant growth (Wani et al., 2008; Khan et al., 2009; GC-MS analysis of the distinctive herbicidal metabolites Sindhu et al., 2018). Five bacterial isolates belonging produced by Pseudomonas aeruginosa H6 was iden­ to Pseudomonas putida (TSAU1), Pseudomonas ex­ tified as quinoline derivatives, which were found highly tremorientalis (TSAU6 and TSAU20), Pseudomonas toxic to the target weeds. Both, supernatant culture and chlo­roraphis (TSAU13) and Pseudomonas aurantiaca crude extract of strain H6 showed high inhibition activity (TSAU22) were selected from the rhizosphere of wheat in Pennisetum purpureum, Oryza sativa, Pisum sativa grown in saline soil (Egamberdieva & Kucharova, and Amaranthus spinosum. 2009). These isolates produced IAA and among these four isolates caused significant increase in the shoot, Production of antibiotics root and dry matter of wheat under saline conditions. Mejri et al. (2010) reported significant gain in growthof The primary mechanism of biocontrol by rhiz­ wheat, barley, oat, pea and chickpea after inoculation with obacteria involves production of antibiotics such as Pseudomonas trivialis strain X33d, whereas inoculation 2,4-diacetylphloroglucinol (DAPG), pyoluteorin, pyrrol­ ­­ of this strain in downy brome weed caused growth nitrin, phenazine-1-carboxyclic acid, 2-hydroxyphe­ ­ inhibition. naz­i­­nes and phenazine-1-carboxamide. Antibiotics have Kennedy et al. (2001) reported stimulation of oilseed also been found to act as determinants in triggering rape growth due to application of P. fluorescens strain in­duced systemic resistance (ISR) in the plant system D7, which aggressively reduced the growth of downy and contribute to disease suppression by conferring a brome. Similarly, Li & Kremer (2006) reported increase competitive advantage to biocontrol agents. Kataryan in growth of soybean and wheat due to application of

Spanish Journal of Agricultural Research December 2019 • Volume 17 • Issue 4 • e10R01 8 Anupma Dahiya, Kavita Chahar and Satyavir S. Sindhu

Figure 2. Inoculation effect of rhizobacterial isolates on growth of wheat and weed (Avena fatua) plants under pot house conditions at 60 days of plant growth. RDF denotes application of recommended doses of fertilizers in the soil for growth of wheat crop.

P. fluorescens strain G2-11. Previously, this strain and MSA56 were found to stimulate growth of wheat, showed suppressive effect on the growth of several whereas isolates MSA39 and WHA87 inhibited the weeds (barnyard grass, green foxtail and morning growth of C. album and isolates MHA75, MHA93 and glory). Certain rhizosphere bacterial strains T42, L9, MSA56 inhibited the growth of A. tenuifolius.

7O0, O010 and W9 were found to be advantageous In another study, rhizobacterial isolates HMM76, under field conditions by causing weed suppression HMM92, JMM24, JMM35 and SYB101 were found to and also improved the competitive ability of the stimulate growth of mustard and inhibited the growth crop against weeds (Abbas et al., 2017). Thus, those of Lathyrus aphaca under pot house conditions (Phour, rhizospheric bacterial isolates that specifically colonize 2016). At 75 days after sowing, inoculation of the two and inhibit growth of weeds but not that of crop plants, bacterial isolates HMM92 and JMM24 showed 54 to may be used as biological control agents. This may 191% increase in RDW and SDW of mustard, whereas benefit agriculture by contributing to increased crop they caused 36 to 92% decrease in RDW and SDW of yields, by reducing weed competition and reducing the Lathyrus aphaca. These rhizobacterial isolates may be use of chemical herbicides (Patil, 2014). further tested for suppression of weed growth under Twelve rhizobacterial isolates were tested for their field conditions for their subsequent application as effect on growth of wheat and weed under pot house bioherbicides. A better understanding of the molecular conditions. Rhizobacterial isolates SYB101, CPS67 biology of plant-microbe interactions may be useful for and HWM11 were found to stimulate growth of wheat designing of strategies in which specific microorganisms and inhibited the growth of Phalaris minor (Phour, may act as PGPR for the cereal and legume crops along 2012). Khandelwal (2016) reported that inoculation with suppressive effects on the growth of weeds. of bacterial isolate WHA87 caused 94-182% increase in RDW and 30-340% increase in SDW of wheat, whereas its inoculation showed 21-81% decrease in Conclusion and future prospects RDW and 33-43% decrease in SDW of Chenopodium album at 30, 60 and 90 days of plant growth under pot Plant rhizosphere is a rich source of nutrients for house conditions. In case of Asphodelus tenuifolius, different microorganisms in the soil (Wen et al., 2017; inoculation of bacterial isolate MSA56 showed 231% Mohanram & Kumar, 2019). These microorganisms increase in RDW and 225% increase in SDW of wheat, in turn, provide different nutrients and hormones for whereas its inoculation caused 40-85.7% decrease in the plant growth, and some of the microbes produce RDW and 53-54.3% decrease in SDW of A. tenuifolius. the metabolites which suppress the growth of weeds Rhizobacterial isolates WHA87, MSA39, MHA75 (Sindhu et al., 2018). The interactions among microbial

Spanish Journal of Agricultural Research December 2019 • Volume 17 • Issue 4 • e10R01 9 Resource partitioning in the rhizosphere for suppression of weed growth: A review

population in the rhizosphere, plant and environment Agbodjato NA, Noumavo PA, Baba-Moussa F, Salami HA, are responsible for the variability observed in growth Sina H, Sèzan A, Baba-Moussa L, 2015. Characterization retardation effects on weeds and in stimulation of plant of potential plant growth promoting rhizobacteria isolated growth. However, the establishment, persistence and from maize (Zea mays L.) in Central and Northern Benin survival of biocontrol agents/bioherbicides in the soil (West Africa). Appl Environ Soil Sci: Art ID 901656. is also a major constraint to their widespread use in https://doi.org/10.1155/2015/901656 commercial agriculture. The continual development of Ahemad M, Khan MS, 2009. 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Spanish Journal of Agricultural Research December 2019 • Volume 17 • Issue 4 • e10R01 13 Resource partitioning in the rhizosphere for suppression of weed growth: A review

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